Factors That Contribute to Blood Loss in Patients With Colonic Angiodysplasia From a Population-Based Study

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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2011;9: Factors That Contribute to Blood Loss in Patients With Colonic Angiodysplasia From a Population-Based Study NAOMI G. DIGGS,* JENNIFER L. HOLUB, DAVID A. LIEBERMAN, GLENN M. EISEN, and LISA L. STRATE Division of Gastroenterology and *Department of Medicine, University of Washington School of Medicine, Seattle, Washington; and Division of Gastroenterology, Department of Internal Medicine, Oregon Health & Science University, Portland, Oregon This article has an accompanying continuing medical education activity on page e49. Learning Objectives At the end of this activity, the learner should distinguish factors that predict blood loss in patients with colonic angiodysplasia. BACKGROUND & AIMS: Most studies of angiodysplasia are small and performed at a single center. We investigated the epidemiology and management of colonic angiodysplasia by using a national endoscopy database. METHODS: Colonoscopy reports (n 229,727; generated from January 2000 to December 2002) from patients with documented angiodysplasia (n 4159) were retrieved from the Clinical Outcomes Research Initiative. Predictors of occult or overt blood loss and endoscopic treatment were identified by using multivariate logistic regression. RESULTS: Most patients with documented angiodysplasia were older than 60 years (73%) or had rightsided lesions (62%). There was evidence of blood loss in 56% of patients with angiodysplasia. Predictors of blood loss included inpatient status (odds ratio [OR], 8.74; 95% confidence interval [CI], ), 2 10 angiodysplasias (OR, 1.50; 95% CI, ), more than 10 lesions (OR, 2.18; 95% CI, ), black race (OR, 1.95; 95% CI, ), severe illness (OR, 1.97; 95% CI, ), Hispanic ethnicity (OR, 1.71; 95% CI, ), and age older than 80 years (OR, 1.32; 95% CI, ). Endoscopic therapy was given to 28% of patients with evidence of blood loss and in 68% with active bleeding. Endoscopic treatment increased among patients in a university practice setting (vs community setting, OR, 2.53; 95% CI, ) and decreased in Northwest geographic locations (vs Southwest, OR, 0.60; 95% CI, ). CONCLUSIONS: Predictors of blood loss in patients with colonic angiodysplasia include inpatient status, comorbidities, age, race/ethnicity, and lesion number. Endoscopic therapy for angiodysplasia varied according to practice setting and region. Keywords: CORI; Lower Gastrointestinal Bleeding; Practice Patterns. View this article s video abstract at Angiodysplasia is an important cause of occult and acute gastrointestinal blood loss, particularly in elderly people. Estimates of prevalence vary from 1% 50% in studies of colonoscopy performed for different indications. 1 9 In studies evaluating severe, ongoing lower intestinal bleeding, angiodysplasia is found in as many as 37% 50% of patients. 7 9 In one study of 964 healthy, asymptomatic patients, angiodysplasia was seen in less than 1%. 10 Angiodysplasia is thought to result from chronic, intermittent, low-grade obstruction of submucosal veins. 11 It might also be a complication of decreased mucosal blood flow and local ischemia. 12 Most lesions are found in the cecum and ascending colon possibly as a result of increased wall tension of the right colon, but angiodysplasia can be found throughout the gastrointestinal tract. 1,6,13 Patients with angiodysplasia are usually older than 60 years of age, with more than a 200-fold increase in incidence between the third and ninth decades of life. 3 This increased incidence with age supports the theory that acquired angiodysplasias are due to degenerative changes. 11 Most colonic angiodyplasias are diagnosed by endoscopy. Colonoscopy has a sensitivity of greater than 80% when the entire colon is examined. 13 Endoscopic therapy for bleeding angiodysplasia is successful, 9,14 18 with a variety of treatment modalities. 18 Therapy is generally indicated only when there is evidence of blood loss or active bleeding from a lesion and not for incidentally found, asymptomatic angiodysplasia. 19 Most studies of angiodysplasia are small and reflect a single center s experience. The aims of this study were to use the Clinical Outcomes Research Initiative (CORI) database to describe the epidemiology and examine the endoscopic treatment practices of colonic angiodysplasia. Methods Clinical Outcomes Research Initiative CORI is a consortium of gastroenterology practices designed to study outcomes of endoscopic procedures in routine practice. The CORI consortium during the study period included 73 gastroenterology practice sites from 27 states including private community practices (71%), university hospitals (17%), and Veterans Affairs hospitals (12%). Participating physicians (525 for this study) use a computerized endoscopic procedure report generator that electronically transmits deidentified reports to a centralized data repository. The data then undergo a series of quality control measures. The CORI database is reviewed annually by the institutional review board at Oregon Health and Science University. Given the use of preexisting, de-identified data, this study was exempt from institu- Abbreviations used in this paper: ASA, American Society of Anesthesiologists; CI, confidence interval; CORI, Clinical Outcomes Research Initiative; OR, odds ratio by the AGA Institute /$36.00 doi: /j.cgh

2 416 DIGGS ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 9, No. 5 tional review board review at the University of Washington (45 CFR (f)). Study Patients We identified all unique patients in CORI who were documented to have at least 1 angiodysplasia during colonoscopic examination between January 1, 2000, and December 31, Patients were excluded if they were younger than 20 years of age or if the endoscopy report noted radiation proctitis and angiodysplasia located in the rectum only (n 103). We collected data entered by the endoscopists including patient demographics, American Society of Anesthesiologists (ASA) classification, exam location (inpatient/outpatient), exam indications, practice type and location, as well as endoscopic findings and treatment. The endoscopic report generator prompts physicians to provide detailed descriptors of angiodysplasia including number, size, location, and whether these lesions were bleeding at the time of the exam. Angiodysplasia number and size (without formal measurement) were estimated by the endoscopists. Details of endoscopic treatment were also collected. In addition, we reviewed 1781 free text comment fields for additional information regarding evidence of blood loss, angiodysplasia characteristics, and endoscopic treatment. Statistical Analysis The main outcomes of interest were evidence of overt or occult blood loss and receipt of endoscopic treatment. Evidence of blood loss was defined as the report of anemia (including iron deficiency anemia), positive fecal occult blood, hematochezia, or melena. We also identified individuals with active bleeding or oozing at the time of colonoscopy. We classified angiodysplasia according to a classification system proposed by Schmit et al 20 that groups lesions according to location (all colon in this study), size ( 2 mm in diameter, 2 5 mm in diameter, 5 mm in diameter), and number (1, 2 10, and 10). We used multivariate logistic regression with backward selection to determine independent predictors of each outcome starting with univariate predictors with a significance level of P.05. Categories were created for missing variables. To assess the importance of provider characteristics, region and site type were added individually to the final model of treatment. We assessed variables with a univariate significance of.1 as potential confounders. We further examined the relationship between age and comorbid disease, given that patients at the extremes of age appeared to be at an increased risk of bleeding (odds ratio [OR] for age years was 1.34 but was not statistically significant). We created cross product terms between dichotomized ASA score ( 3 vs 3) and each of the age categories, and these terms were added to the multivariable model. We present the adjusted ORs and 95% confidence intervals (CIs). A P value of.05 was considered statistically significant. We performed all analyses by using SAS, Version 9.2 (SAS Institute, Cary, NC). Table 1. Baseline Characteristics of Individuals With Colonic Angiodysplasia Characteristic Total, n 4159 (%) Bleeding, a n 2320 (%) Exam indication No bleeding, n 1839 (%) Age (y) (2.5) 65 (2.8) 39 (2.1) (25) 559 (24) 460 (25) (58) 1285 (55) 1109 (60) (15) 411 (18) 231 (13) Male 2267 (55) 1273 (55) 994 (54) Race/ethnicity White 3590 (86) 1970 (85) 1620 (88) Black 244 (6) 171 (7.4) 73 (4) Hispanic 311 (7.5) 213 (9.2) 98 (5.3) Other 62 (1.5) 38 (1.6) 24 (1.3) Unknown 263 (6.3) 141 (6) 122 (6.6) ASA class I 948 (25) 454 (21) 494 (29) II 2232 (58) 1196 (56) 1036 (61) III 605 (16) 441 (21) 164 (10) IV 36 (0.08) 30 (1.4) 6 (0.35) Unknown 338 (8) 199 (8.6) 139 (7.6) Inpatient exam 266 (6.4) 247 (11) 19 (1) Exam site Community 2851 (69) 1544 (67) 1307 (71) University 628 (15) 341 (15) 287 (16) Veterans Affairs 592 (14) 391 (17) 201 (11) Other 88 (2) 44 (2) 44 (2) US region North Central 316 (8) 155 (7) 161 (9) Northeast 883 (21) 486 (21) 397 (22) Northwest 510 (12) 303 (13) 207 (11) South Central 391 (9) 271 (12) 120 (7) Southeast 526 (13) 315 (14) 211 (11) Southwest 1532 (37) 790 (34) 742 (40) a Overt or occult bleeding including hematochezia, melena, anemia, or positive fecal occult blood. Results Of the 229,727 colonoscopies performed between January 2000 and December 2002, 4159 patients (1.8%) were documented to have angiodysplasia. Table 1 summarizes the baseline characteristics and demographics of patients. A majority of the patients (73%) were older than 60 years, 55% were male, and 86% were white. Severe comorbid illness (ASA class III) was present in 16% of cases. Other findings on colonoscopy in addition to angiodysplasia included diverticula (54%), polyps (40%), colitis (4%), and malignancy (0.8%). A majority of colonoscopies in patients with colonic angiodysplasia were performed as outpatients (84%) in community-based practices (69%). Fifteen percent of colonoscopies were performed in a university hospital and 14% in a Veterans Administration hospital. Of the 4159 patients with colonic angiodysplasia, 2320 (56%) were noted to have evidence of occult or overt blood loss including 1 or more of the following indications for colonoscopy: hematochezia (41%), anemia (37%, including iron deficiency anemia in 2%), positive fecal occult blood test (33%), or melena (7%). The characteristics of the angiodysplastic lesions are described in Table 2 by using a modification of a previously proposed endoscopic classification scheme. 20 Forty-one percent of angiodysplasias were solitary, 30% were multiple (2 10 lesions), and 9% were diffuse (more than 10 lesions). Half of angiodysplasias were estimated to be intermediate in size, rang-

3 May 2011 POPULATION-BASED STUDY OF COLONIC ANGIODYSPLASIA 417 Table 2. Characteristics of Colonic Angiodysplasia Characteristic n (%) a Number Unique (1) 1898 (41) Multiple (2 10) 1376 (30) Diffuse ( 10) 407 (9) Unknown 935 (20) Size (mm) Minute ( 2) 112 (3) Intermediate (2 5) 2311 (50) Large ( 5) 891 (19) Unknown 1302 (28) Location Cecum 1789 (40) Ascending 1002 (22) Transverse 331 (7) Descending 1068 (24) Rectum 278 (6) Active bleeding 328 (7) a Providers were able to enter multiple lines of data for a single patient. For 4159 unique patients, there were 4616 separate records of angiodysplasia. Table 4. Multivariable Analysis of Factors Associated With Endoscopic Treatment of Colonic Angiodysplasia Characteristic Adjusted OR (95% CI) P value Age (y) ( ) Reference group ( ) ( ).008 Size (mm) ( ) Reference group ( ).0001 Location Left colon 1.0 Reference group Transverse 1.04 ( ).88 Right colon 1.54 ( ).0003 Evidence of bleed a 5.36 ( ).0001 Active bleeding ( ).0001 Inpatient 2.52 ( ).0001 a Overt or occult bleeding including hematochezia, melena, anemia, or positive fecal occult blood. ing from 2 5 mm. Twenty percent of lesions were larger than 5 mm. Sixty-two percent of angiodysplasias were found in the cecum and ascending colon. Active bleeding from angiodyplasia was reported in 328 cases (7%). In the multivariable analysis, factors associated with evidence of overt or occult blood loss in patients with colonic angiodysplasia included inpatient status, age older than 80 years, severe comorbid illness (ASA class III), black race, Hispanic ethnicity, and multiple or diffuse lesions (Table 3). Forward and backward selection identified the same independent predictors. Multivariable analysis of active bleeding seen at endoscopy identified similar predictors, with the addition of Table 3. Multivariable Analysis of Factors Associated With Evidence of Overt or Occult Blood Loss in Patients With Colonic Angiodysplasia Characteristic Adjusted OR (95% CI) P value Inpatient exam 8.74 ( ).0001 Age (y) ( ) Reference group ( ) ( ).01 Race White 1.0 Reference group Black 1.95 ( ).0001 Other 1.31 ( ).33 Ethnicity Not Hispanic 1.0 Reference group Hispanic 1.71 ( ).0001 ASA class I, II 1.0 Reference group III, IV 1.97 ( ).0001 Number Reference group ( ) ( ).0001 right-sided location (OR, 1.85; 95% CI, ; P.001) and lesion size greater than 5 mm (OR, 1.38; 95% CI, ; P.048). In addition, race and ethnicity were not predictive of active bleeding. The interaction between ASA score and age years was significant in the multivariable model of blood loss (P.007), and between ASA score and age 80 years was of borderline significance (P.059). We also stratified the analysis by ASA score ( 3 vs 3) and found that in patients with a high ASA score, the relationship between age and bleeding was more linear in nature; patients 40 years of age were not at increased risk of bleeding (OR, 0.59; 95% CI, ), patients years were at moderate risk (OR, 1.66; 95% CI, ), and patients 80 years were at the highest risk (OR, 2.35; 95% CI, ), although the confidence interval was wide for young patients. A total of 17% of patients with documented angiodysplasias were treated endoscopically. Endoscopic treatment of angiodysplasia was used in 27% of patients with evidence of overt or occult blood loss. Sixty-eight percent of actively bleeding angiodysplasias were treated, as were 47% of angiodysplasias in hospitalized patients with hematochezia. Five percent of patients without an indication of blood loss received endoscopic treatment. The most common treatment modality was thermal coagulation (62%), followed by argon plasma coagulation (17%), injection with epinephrine and/or saline (3.2%), and the use of both injection and thermal coagulation (2.4%). In the multivariable analysis, predictors of treatment included patients with evidence of blood loss, active bleeding at the time of endoscopy, young (20 39 years) and very old ( 80 y) age, inpatient status, size 5 mm, and right-sided location (Table 4). The same independent predictors were identified by using a forward selection process. Treatment was more likely to occur at a university site (adjusted OR, 2.53; 95% CI, ); P.001) than at a community site. Lesions were less likely to be treated in the Northwest (adjusted OR, 0.60; 95% CI, ; P.003) than in the Southwest. Independent predictors of receipt of

4 418 DIGGS ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 9, No. 5 endoscopic treatment for actively bleeding lesions were size 5 mm (OR, 3.47; 95% CI, ; P.005) and inpatient exam (OR, 4.30; 95% CI, ; P.005). Patients with more than 10 lesions were less likely to receive treatment for active bleeding (OR, 0.36; 95% CI, ); P.018). Discussion To our knowledge, this is the largest study of patients with angiodysplasia reported to date. Data from more than 70 practice sites across the United States provide a unique population-based perspective and enable the analysis of treatment practices. Of more than 200,000 colonoscopies performed for various indications, 2% of patients were found to have colonic angiodysplasia. This finding confirms that angiodysplasia is a relatively infrequent colonoscopic finding. 3,4,6,10 We did not examine angiodysplasia in the context of acute lower intestinal bleeding or in elderly people specifically, but we presume that the prevalence in these select populations would be higher than that seen in all patients undergoing colonoscopy. The highest prevalence of angiodysplasia (40% 50%) is reported in studies of patients with severe, ongoing hematochezia. 7 9 As in previous studies, a majority of lesions were located in the right colon, supporting the role of increased wall tension in the pathogenesis of angiodysplasia. In our study, a majority of patients with angiodysplasia were older than 60 years of age. This might reflect the fact that most patients undergoing colonoscopy are older than 50 years of age, and we did not have data on individuals without angiodysplasia with which to compare. Nonetheless, our findings are consistent with the literature and suggest that angiodysplasia is an age-related degenerative lesion. Indeed, more than half of patients with angiodysplasia also had diverticulosis, a condition that similarly occurs with aging. We examined risk factors associated with blood loss in patients with documented angiodysplasia. We recognize that use of nonsteroidal anti-inflammatory drugs or anticoagulation could promote bleeding from these lesions. In this analysis, we did not have accurate information about drug use. What we report are important patient characteristics that were linked to bleeding. We found that in patients with colonic angiodysplasia, inpatient status, advanced age, comorbid illnesses, black race, Hispanic ethnicity, and the presence of multiple lesions were associated with evidence of blood loss. We suspect that antiplatelet or anticoagulants might be more likely to promote bleeding in these higher-risk patients. The majority of patients with angiodysplasia had concomitant comorbid illness, and severe comorbidity, as assessed by ASA class, was a predictor of bleeding. In addition, we found a significant interaction between age and comorbid illness and blood loss, suggesting that the interplay of age and illness is important. An increased incidence of angiodysplasia has been described with a number of comorbid illnesses including aortic stenosis, renal failure, von Willebrand s disease, cirrhosis, and pulmonary disease. 19 It remains to be determined whether these illnesses increase the risk of blood loss and thus the detection of angiodysplasia (eg, via coagulopathy or platelet dysfunction), or whether they are involved in the development of angiodysplasia through mechanisms such as ischemia. We also noted that patients with multiple ( 10) lesions were more likely to have evidence of blood loss, and patients with large lesions ( 5 mm) were more likely to have active bleeding at the time of colonoscopy. Patients with multiple lesions would be expected to have a cumulatively higher risk of blood loss from each lesion. As for the association between larger angiodysplasias and bleeding, we speculate that the local factors that influence the development of these vascular lesions (obstruction of submucosal veins, ischemia, increased wall tension 11,12 ) might be even more pronounced in larger lesions and might increase the chance of bleeding. It is also possible that larger or multiple lesions were simply more likely to be seen or recorded by the endoscopist. This study suggests a relationship between race and ethnicity and angiodysplasia. These findings might indicate an inherited tendency for angiodysplasia formation or bleeding or perhaps reflect a higher prevalence of other risk factors that were not accounted for in our adjusted analysis. For example, chronic kidney disease is more prevalent among black and Hispanic populations 21 and might confer increased bleeding risk via platelet dysfunction or vascular disease. Importantly, we could not account for sociodemographic factors in our analysis. The study of race and disease is complex and deserves further investigation in the context of angiodysplasia. Our findings suggest that endoscopic treatment of angiodysplasia is inconsistent across regions, practice settings, and clinical scenarios. A total of 27% of patients with any evidence of blood loss and 68% with actively bleeding lesions received endoscopic treatment. Although this might be suggestive of incomplete data acquisition, we speculate that the use of endoscopic treatment is an important element of the endoscopy report and is unlikely to be omitted if performed. Furthermore, to account for differences in endoscopic reporting practices, we reviewed all comment or free text fields within the endoscopic reports. This process identified 57 additional patients with active bleeding and 227 who received endoscopic treatment. Nonetheless, our data are limited to the colonoscopic encounter, and we might not have accounted for credible reasons for withholding endoscopic therapy such as coagulopathy or other sources of blood loss (eg, an upper tract source in a patient also found to have nonbleeding colonic angiodysplasia). However, the latter reason would not account for failure to treat actively bleeding angiodysplasia. Another explanation for the variation in treatment practices could be the lack of conviction among endoscopists that treating isolated angiodysplastic lesions, particularly in patients with chronic anemia, will have significant clinical impact. Angiodysplasia might be present elsewhere in the gastrointestinal tract and tend to recur after treatment. Furthermore, treatment of incidentally noted lesions lacks convincing outcomes data. Endoscopic therapy was less likely to be used in community practice and in the Northwest. Patients with more comorbid illness, and thus more likely to have bleeding, might be seen preferentially in an academic setting, although the multivariable model was adjusted for age, ASA classification, and presence of active bleeding. We also speculate that the case loads might be lighter in the academic setting, and this might facilitate endoscopic treatment, especially when several lesions are present. Overutilization of therapy in the university setting or in the Southwest cannot be excluded. However, we would have expected financial incentives to favor treatment in the community setting. The reasons for regional variation in treatment practices are not clear but might reflect differences in the training of endoscopists and their perceptions as to the utility of treating angiodysplasia.

5 May 2011 POPULATION-BASED STUDY OF COLONIC ANGIODYSPLASIA 419 A primary strength of this study is the large population of more than 4000 patients with angiodysplasia. Data were gathered on the vast majority of patients from each practice site by using the standardized CORI report generator designed for research purposes. Because we examined all angiodysplasias and not just those found in colonoscopies performed for acute hematochezia, we were able to broadly describe the epidemiology and risk factors for bleeding in colonic angiodysplasia. The variety of practice settings across the United States also enabled us to evaluate treatment practices. Our study has several important limitations. The retrospective data are limited to the endoscopy encounter, and thus specifics such as the presence of comorbid illness (beyond ASA class), contraindications to therapy, potential confounding variables, other sources of blood loss, or previous endoscopic treatment are not available for analysis. These factors likely account in part for the apparent infrequent use of endoscopic therapy particularly in patients without active bleeding at the time of colonoscopy. In addition, variation in endoscopic reporting might have led to misclassification, although we accounted for all comment and free text fields. There might also have been a tendency for endoscopists to report the presence of angiodysplasia in those patients with evidence of blood loss as opposed to those undergoing screening colonoscopy. Therefore, the true incidence of angiodysplasia might be higher than reported, whereas the prevalence of blood loss in patients with angiodysplasia might be overstated. We also rely on the accuracy of endoscopic interpretation as to the presence or absence of angiodyplasia and the size and number of lesions because neither photo nor video confirmation is available in this retrospective analysis. We were unable to assess the prevalence of angiodysplasia in specific populations such as those with acute hematochezia or in specific age groups. In the subanalyses of active bleeding and endoscopic treatment, smaller numbers of outcomes might have affected the stability of the multivariable models. Last, the use of aspirin, nonsteroidal anti-inflammatory drugs, or other anticoagulants is an important potential confounder that we were unable to account for in our analysis, and that could alter the associations seen between variables such as age and comorbid disease and bleeding. In summary, our results show that angiodysplasia is an uncommon finding in all patients undergoing colonoscopy. Older patients with angiodysplasia and those with comorbid illness or multiple lesions are more likely to have evidence of blood loss. Endoscopic treatment is appropriately reserved for symptomatic patients, but treatment of patients with overt or occult bleeding is inconsistent. Variations in endoscopic treatment practices point to the need for prospective studies to develop a more standardized approach to the treatment of colonic angiodysplasia. Supplementary Material Note: To access the supplementary material accompanying this article, visit the online version of Clinical Gastroenterology and Hepatology at and at doi: / j.cgh References 1. Hochter W, Weingart J, Kuhner W, et al. Angiodysplasia in the colon and rectum: endoscopic morphology, localisation and frequency. Endoscopy 1985;17: Richter JM, Christensen MR, Kaplan LM, et al. Effectiveness of current technology in the diagnosis and management of lower gastrointestinal hemorrhage. Gastrointest Endosc 1995;41: Longstreth GF. Epidemiology and outcome of patients hospitalized with acute lower gastrointestinal hemorrhage: a populationbased study. Am J Gastroenterol 1997;92: Rockey DC, Koch J, Cello JP, et al. Relative frequency of upper gastrointestinal and colonic lesions in patients with positive fecal occult-blood tests. N Engl J Med 1998;339: Heer M, Sulser H, Hany A. Angiodysplasia of the colon: an expression of occlusive vascular disease. Hepatogastroenterology 1987;34: Danesh BJ, Spiliadis C, Williams CB, et al. Angiodysplasia: an uncommon cause of colonic bleeding colonoscopic evaluation of 1,050 patients with rectal bleeding and anaemia. Int J Colorectal Dis 1987;2: Jensen DM, Machicado GA. Diagnosis and treatment of severe hematochezia: the role of urgent colonoscopy after purge. Gastroenterology 1988;95: Jensen DM, Machicado GA. Colonoscopy for diagnosis and treatment of severe lower gastrointestinal bleeding: routine outcomes and cost analysis. Gastrointest Endosc Clin N Am 1997;7: Santos JC Jr, Aprilli F, Guimaraes AS, et al. Angiodysplasia of the colon: endoscopic diagnosis and treatment. Br J Surg 1988;75: Foutch PG, Rex DK, Lieberman DA. Prevalence and natural history of colonic angiodysplasia among healthy asymptomatic people. Am J Gastroenterol 1995;90: Boley SJ, Sammartano R, Adams A, et al. On the nature and etiology of vascular ectasias of the colon: degenerative lesions of aging. Gastroenterology 1977;72: Baum S, Athanasoulis CA, Waltman AC, et al. Angiodysplasia of the right colon: a cause of gastrointestinal bleeding. AJR Am J Roentgenol 1977;129: Richter JM, Hedberg SE, Athanasoulis CA, et al. Angiodysplasia: clinical presentation and colonoscopic diagnosis. Dig Dis Sci 1984;29: Davila RE, Rajan E, Adler DG, et al. ASGE guideline: the role of endoscopy in the patient with lower-gi bleeding. Gastrointest Endosc 2005;62: Olmos JA, Marcolongo M, Pogorelsky V, et al. Long-term outcome of argon plasma ablation therapy for bleeding in 100 consecutive patients with colonic angiodysplasia. Dis Colon Rectum 2006; 49: Rutgeerts P, Van Gompel F, Geboes K, et al. Long term results of treatment of vascular malformations of the gastrointestinal tract by neodymium Yag laser photocoagulation. Gut 1985;26: Kwan V, Bourke MJ, Williams SJ, et al. Argon plasma coagulation in the management of symptomatic gastrointestinal vascular lesions: experience in 100 consecutive patients with long-term follow-up. Am J Gastroenterol 2006;101: Eisen GM, Dominitz JA, Faigel DO, et al. An annotated algorithmic approach to acute lower gastrointestinal bleeding. Gastrointest Endosc 2001;53: Sharma R, Gorbien MJ. Angiodysplasia and lower gastrointestinal tract bleeding in elderly patients. Arch Intern Med 1995;155: Schmit A, Van Gossum A. Proposal for an endoscopic classification of digestive angiodysplasias for therapeutic trials: the European Club of Enteroscopy. Gastrointest Endosc 1998;48: Collins AJ. Excerpts from the United States Renal Data System 2008 annual data report. Am J Kidney Dis 2009;53:S1 S374. Reprint requests Address requests for reprints to: Lisa L. Strate, MD, MPH, Harborview Medical Center, 325 Ninth Avenue, Box , Seattle, Washington lstrate@uw.edu; fax: (206)

6 420 DIGGS ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 9, No. 5 Conflicts of interest The authors disclose the following: Dr Lieberman is the executive director and Dr Eisen is the executive codirector of CORI, a nonprofit organization that receives funding from federal and industry sources. This potential conflict of interest has been reviewed and managed by the Oregon Health & Science University (OHSU) Conflict of Interest in Research Committee. The remaining authors disclose no conflicts. Funding This study was funded by grants from the AHRQ (K08 HS14062) (L.L.S.), the American Society for Gastrointestinal Endoscopy (L.L.S.), the NIDDK UO1 U01DK57132 and R33-DK In addition, the practice network (Clinical Outcomes Research Initiative [CORI]) has received support from the following entities to support the infrastructure of the practice-based network: AstraZeneca, Bard International, Pentax, USA, ProVation, Endosoft, GIVEN Imaging, and Ethicon.

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